Pine Voles Research Articles

Rediscovery of the Bavarian pine vole (Microtus bavaricus) in Germany

Abstract We report the rediscovery of Microtus bavaricus in Germany, a small mammal that had not been recorded here in more than 60 years. Between 2012 and 2014, a citizen science project addressed cat owners and farmers to collect rodents killed by cats and traps. Until 2017, we conducted 3,432 live trap nights to rediscover the species in and around the area of its discovery. However, only a three-step approach (screening large areas for the occurrence of pine voles using camera trapping, live trapping for collecting genetic material, DNA-barcoding) allowed for the rediscovery of this elusive species near Mittenwald in 2023.

Detection of hepatitis E virus genotype 3 in an Algerian mouse (Mus spretus) in Portugal

Virus monitoring in small mammals is central to the design of epidemiological control strategies for rodent-borne zoonotic viruses. Synanthropic small mammals are versatile and may be potential carriers of several microbial agents. In the present work, a total of 330 fecal samples of small mammals were collected at two sites in the North of Portugal and screened for zoonotic hepatitis E virus (HEV, species Paslahepevirus balayani). Synanthropic small mammal samples (n = 40) were collected in a city park of Porto and belonged to the species Algerian mouse (Mus spretus) (n = 26) and to the greater white-toothed shrew (Crocidura russula) (n = 14). Furthermore, additional samples were collected in the Northeast region of Portugal and included Algerian mouse (n = 48), greater white-toothed shrew (n = 47), wood mouse (Apodemus sylvaticus) (n = 43), southwestern water vole (Arvicola sapidus) (n = 52), Cabrera’s vole (Microtus cabrerae) (n = 49) and Lusitanian pine vole (Microtus lusitanicus) (n = 51). A nested RT-PCR targeting a part of open reading frame (ORF) 2 region of the HEV genome was used followed by sequencing and phylogenetic analysis. HEV RNA was detected in one fecal sample (0.3%; 95% confidence interval, CI: 0.01–1.68) from a synanthropic Algerian mouse that was genotyped as HEV-3, subgenotype 3e. This is the first study reporting the detection of HEV-3 in a synanthropic rodent, the Algerian mouse. The identified HEV isolate is probably the outcome of either a spill-over infection from domestic pigs or wild boars, or the result of passive viral transit through the intestinal tract. This finding reinforces the importance in the surveillance of novel potential hosts for HEV with a particular emphasis on synanthropic animals.

Екологія полівки підземної (Microtus subterraneus) у високогір’ї Українських Карпат

The article presents information on the ecology of pine voles in the highlands of the Carpathians based on the results of studies conducted in 1956–1986. The results of population surveys in different types of habitats and plant associations are presented, with corresponding estimates of abundance (maximum 123 specimens/ha) and density (maximum 2.6 kg/ha), as well as an analysis of population features in different habitats and different years. The high frequency of the species occurrence in ruderal coenoses of the highlands, in particular in thickets of the alpine sorrel, is shown. Detailed information on the reproduction of populations, in particular on the number of young in a litter, is given: the modal value is 2–3, the limits are 1–5, and the average is 2.4–2.9, depending on the biotope (plant association). Data on the ratio of reproductively active individuals and the age and sex structure of populations, as well as the ecomorphological and ecophysiological parameters of voles are presented.

Designers of Nature's Subterranean Abodes: Insights into the Architecture and Utilization of Burrow Systems of Thomas' Pine Vole, Microtus thomasi (Rodentia: Arvicolinae).

Microtus thomasi (Rodentia: Arvicolinae), a fossorial vole endemic to the SW Balkans, uses a variety of substrates but its underground behavior remains poorly understood. This study examines the architecture and utilization of M. thomasi burrow systems in NW Peloponnese, Greece. In particular, eight burrow systems were meticulously excavated and studied, with comprehensive measurements taken of key characteristics, including length, depth, soil mounds, and surface openings. Key coordinates were recorded using a differential GPS device for detailed mapping and fractal dimension analysis using the box-counting method was employed to assess burrow system complexity. Soil samples were analyzed for particle size and chemical composition, and vegetation types at each site were identified. We did not find statistically significant correlations between size and complexity of the burrow systems and soil composition, altitude, or specific soil components. On the other hand, we did observe statistically significant differences in tunnel diameter between two burrow systems and in tunnel depth between more. Moreover, our study showed that more than one same-sex individual can occupy a single burrow system and not just an adult male-female pair, that was previously recorded, indicating the need for further study of the social behavior of this vole species. This study provides valuable insights into the underground behavior of M. thomasi by providing information on the features of its burrow systems, thus contributing to our understanding of its biology.

Prevalence of Ectoparasites on Small Mammals Inhabiting an Agroforestry System of Western Portugal

The goal of this study was to assess ectoparasite-small mammal host associations in central-west Portugal in native and exotic habitats, respectively, including a cork oak woodland and a Eucalyptus plantation. Mammals were sampled with Sherman and pitfall traps, and ectoparasites were collected and identified in all samples. We trapped 681 small mammals: 5 rodent species - wood mouse, Apodemus sylvaticus (N = 527); the Algerian mouse, Mus spretus (N = 67); Cabrera's vole, Microtus cabrerae (N = 8); the Lusitanian pine vole, Microtus lusitanicus (N = 2); and the black rat, Rattus rattus (N = 1) - and 1 insectivore species - the greater white-toothed shrew, Crocidura russula (N = 76). We identified 4 flea species (Nosopsyllus fasciatus, Ctenophthalmus sp., Typhloceras favosus, and Typhloceras poppei); 5 tick species (Haemaphysalis punctata, Ixodes ricinus, Ornithodoros sp., Rhipicephalus pusillus, and Rhipicephalus sanguineus); and 1 chigger species (Neotrombicula sp.) from hosts. The wood mouse was the small mammal species with the highest overall ectoparasite prevalence, although ticks were the least prevalent taxon. We found that ectoparasite guilds represented a somewhat generalist host pattern, and chiggers presented some host specificity. The data presented herein increase the knowledge regarding ectoparasite prevalence and distribution among small mammal hosts in the Mediterranean. Although surveys of ectoparasites of small mammals in central-west Portugal are not novel, this is the first time that a species belonging to the genus Ctenophthalmus is reported from M. cabrerae (Cabrera's vole) in Portugal.

Molecular assessment of the taxonomic status of pine vole species Microtus subterraneus and Microtus majori in southeastern Europe and Turkey

Intra– and inter–specific phylogenetic relationships and the taxonomic status of pine vole populations have been controversial for years, and cryptic species are thought to exist, especially concering the species' distribution area. To clarify the taxonomic status of Turkish populations we analysed mitochondrial (cytochrome–b and cytochrome oxidase–I) and nuclear (interphotoreceptor retinoid binding protein) gene markers, adding GenBank data from Europe and Caucasia. Considering the data obtained based on mean genetic distance, genetic diversity and fixation index values, Bayesian trees and Median–joining networks, we found that M. subterraneus and M. majori are valid species which have diverged since 1.28 Mya. Findings also suggested that although Anatolian, Thracian (Turkish Thrace and Greece) and European populations of M. subterraneus and Anatolian and Caucasian populations of M. majori have been in the process of divergency since 0.528–0.337 Mya correspond to the Pleistocene glacial periods, these intrapopulations do not appear to be different species.Besides, considering the high intraspecific variation in M. subterraneus, it remains likely that new species could be identified in future studies.

Detection and Molecular Characterization of Giardia and Cryptosporidium spp. Circulating in Wild Small Mammals from Portugal.

Cryptosporidium spp. and Giardia spp. are important diarrhea-causing protozoan parasites worldwide that exhibit broad host ranges. Wild small mammals can harbor host-adapted and potentially zoonotic species of both parasites. The aim of this study was to investigate Cryptosporidium spp. and Giardia spp. in wild rodents and shrews in Portugal, focusing on the protist's occurrence and genetic diversity. Molecular screening by PCR at the small subunit (SSU) rRNA gene locus of 290 fecal samples from wood mice (Apodemus sylvaticus), southwestern water voles (Arvicola sapidus), Cabrera's voles (Microtus cabrerae), Lusitanian pine voles (Microtus lusitanicus), Algerian mice (Mus spretus) and greater white-toothed shrews (Crocidura russula) in Northeast Portugal revealed the low occurrence of Cryptosporidium spp. (1%) and high occurrence of Giardia spp. (32.8%). The analysis revealed that "species" was the only significant factor associated with the increasing probability of Giardia spp. infection, with the highest prevalence reported in southwestern water voles and Lusitanian pine voles. Cryptosporidium and Giardia species determination at the SSU rRNA gene locus revealed C. muris and G. microti as the only circulating species, respectively. Subtyping of the glutamate dehydrogenase (gdh) and beta-giardin (bg) genes provided evidence of the high genetic diversity within the G. microti clade. This study suggests that rodent-adapted G. microti occurs to a large extent in cricetid hosts and supports the limited role of wild rodents and shrews as natural sources of human infections in Northeast Portugal regarding the investigated parasites. Moreover, this is the first record of G. microti in southwestern water voles, Lusitanian pine voles, Algerian mice, wood mice and Cabrera's voles and C. muris in Cabrera's voles. Finally, this study improves the database of sequences relevant for the sequence typing of G. microti strains and provides new insights about the epidemiology of Giardia spp. and Cryptosporidium spp. in wild rodents and shrews, two parasite genera of high importance for public and animal health.

Small mammals in the diet of the tawny owl Strix aluco in selected sites of the Biebrza Basin and Knyszyn Forest in north-eastern Poland.

The analysis of pellets of the tawny owl Strix aluco collected in the years 2009–2023 in 22 sites (ten in the Biebrza Basin and twelve in Knyszyn Forest) allowed for finding four species of Soricomorpha, nine species of Chiroptera and fifteen species of Rodentia (4, 5 and 12 in the Biebrza Basin and 4, 7 and 13 in Knyszyn Forest, respectively). Most common and most frequently caught by owls were: the bank vole Clethrionomys glareolus, the yellow-necked mouse Apodemus flavicollis and the common shrew Sorex araneus. Valuable species of bats included the pond bat Myotis dasycneme and the western barbastelle Barbastella barbastellus noted in Knyszyn Forest. Rare rodents found in both study areas were: the northern birch mouse Sicista betulina and the common dormouse Muscardinus avellanarius while the forest dormouse Dryomys nitedula was noted only in Knyszyn Forest. The European water vole Arvicola amphibius commonly noted in the Biebrza Basin was not found in Knyszyn Forest. On the contrary, the common pine vole Microtus subterraneus was reecorded only in Knyszyn Forest.

Adaptive responses of the pine vole (Microtus subterraneus) population to anthropogenic environmental changes

Adaptive responses of the pine vole (Microtus subterraneus) population to anthropogenic environmental changes

Distribution of Four Vole Species through the Barn Owl Tyto alba Diet Spectrum: Pattern Responses to Environmental Gradients in Intensive Agroecosystems of Central Greece.

Voles are the most common vertebrate pests in European agriculture. Identifying their distribution and abundance patterns provides valuable information for future management. Barn Owl diet analysis is one of the optimum methods used to record small mammal distribution patterns on large spatial scales. From 2003 to 2005, a total of 10,065 Barn Owl pellets were collected and analyzed from 31 breeding sites in the largest agroecosystem in Greece, the Thessaly plains. A total of 29,061 prey items were identified, offering deep insight into small mammal distribution, specifically voles. Four discrete vole species (Harting's vole Microtus hartingi, East European vole Microtus levis, Thomas's pine vole Microtus thomasi, and Grey dwarf hamster Cricetulus migratorius) comprised 40.5% (11,770 vole prey items) of the total Barn Owl prey intake. The presence and abundance of the voles varied according to underlying environmental gradients, with soil texture and type playing a major role. M. levis showed no significant attachments to gradients, other than a mild increase in Mollisol soils. It was syntopic in all sites with M. hartingi, which was the dominant and most abundant small mammal species, preferring non-arable cultivated land, natural grasslands, set-aside fields, and fallow land. M. thomasi was strictly present in western Thessaly and strongly associated with a sandy-clay soil texture and Alfisol soils. C. migratorius was the least represented vole (162 items), exclusively present in eastern Thessaly and demonstrating a stronger association with cereals, Mollisol soils, and an argillaceous-clay soil texture. This is the first study in Greece at such a large spatial scale, offering insights for pest rodents' distribution in intensive agroecosystems and their response to environmental gradients including soil parameters.

COI gene analyses of the Daghestan pine vole (Microtus daghestanicus Shidlovsky, 1919) population from northeastern Turkey

Daghestan pine vole (Microtus daghestanicus Shidlovsky, 1919) is spread in Caucasia, Turkey and Northwestern Iran and distribution of this species is limited to Northeastern Anatolia in Turkey. Few molecular studies on M. daghestanicus have been performed so far, and it was analysed in this study with the mitochondrial cytochrome oxidase subunit I (COI) region and compared with other Terricola species (Microtus subterraneus and Microtus majori) and other Microtus species found in its distribution area (Microtus arvalis and Microtus mystacinus). For this purpose, mean genetic distance values and fixation index values were calculated. Also, Bayesian Inference tree and Median-joining network were constructed. The acquired results showed that M. daghestanicus was clearly separated in the Pleistocene Period and was closer to M subterraneus than M. majori in the subgenus Terricola.

Hunger sweetens the beans: evidence of opportunistic feeding behaviour of the little owl (Athene noctua, Scopoli 1769) from Peloponnese, Greece

Abstract The little owl (Athene noctua) is a common raptor in Mediterranean habitats. To acquire more information on its diet, this study identified cranial and post-cranial skeletal material from 70 owl pellets collected during the 2016 and 2017 breeding seasons. The material was used to quantify the little owl’s relative prey abundance using MNI (minimum number of individuals), a taphonomical unit. This study is the first to examine the diet of the little owl in the Peloponnese (southern Greece). After examining 3,691 isolated skeletal and exoskeletal remains from the processed pellets, a total of 78 and 108 prey items were recorded for the two consecutive years. This study, in congruence with previous research, showed that in both years the little owl favoured primarily small mammals and arthropods, with a clear predominance of Thomas’s pine vole (Microtus thomasi) and arthropods from the class Diplopoda. Finally, a redundancy discriminant analysis (RDA) was applied to our two-year results, along with those from similar studies in the Mediterranean region, to examine the relationship between habitat types and prey taxa, which supported the little owl’s opportunistic feeding behaviour, depending on variation of ecological factors.

Microplastic contamination in terrestrial ecosystems: A study using barn owl (Tyto alba) pellets

Microplastics (MPs) are recognised as an emerging environmental problem that needs to be carefully monitored. So far, MPs have been widely recorded in marine and freshwater ecosystems. Still, few studies have focused on MP occurrence in terrestrial ecosystems, although soils are suspected to be one of the main MP reservoirs. To test a non-invasive method for assessing MP contamination in terrestrial ecosystems, we analysed the pellets of a top terrestrial predator, the barn owl (Tyto alba). Sixty pellets were collected from three agricultural areas (20 pellets each) and analysed to assess both barn owl diet and MP content. Thirty-four MPs were confirmed by micro-Fourier Transform Infrared Spectroscopy (μ-FTIR) analysis in 33% of the pellets (min-max 1–5 MPs per pellet). Most of the detected items were microfibres (88.2%). Polyethylene terephthalate, polyacrylonitrile and polyamide were the most abundant polymers. One of the three sites was significantly less contaminated. In the two sites with the highest MP occurrences, barn owl diet was characterised by predation on synanthropic rodents, particularly brown rats (Rattus norvegicus), which may indicate habitat degradation and increased exposure to MPs. Analyses also suggest that Savi's pine vole (Microtus savii) is the prey least at risk of MP contamination, probably due to its strictly herbivorous diet. We argue that the analysis of barn owl pellets may represent a cost-effective method for monitoring MP contamination in terrestrial ecosystems.

Cell adhesion and immune response, two main functions altered in the transcriptome of seasonally regressed testes of two mammalian species.

In species with seasonal breeding, male specimens undergo substantial testicular regression during the nonbreeding period of the year. However, the molecular mechanisms that control this biological process are largely unknown. Here, we report a transcriptomic analysis on the Iberian mole, Talpa occidentalis, in which the desquamation of live, nonapoptotic germ cells is the major cellular event responsible for testis regression. By comparing testes at different reproductive states (active, regressing, and inactive), we demonstrate that the molecular pathways controlling the cell adhesion function in the seminiferous epithelium, such as the MAPK, ERK, and TGF-β signaling, are altered during the regression process. In addition, inactive testes display a global upregulation of genes associated with immune response, indicating a selective loss of the "immune privilege" that normally operates in sexually active testes. Interspecies comparative analyses using analogous data from the Mediterranean pine vole, a rodent species where testis regression is controlled by halting meiosis entry, revealed a common gene expression signature in the regressed testes of these two evolutionary distant species. Our study advances in the knowledge of the molecular mechanisms associated to gonadal seasonal breeding, highlighting the existence of a conserved transcriptional program of testis involution across mammalian clades.

Genetic Diversity of Species of Microtus Generic Group (Arvicolinae, Rodentia): New Data from the Greater Caucasus.

Using the cytochrome b gene (1143 bp), species identification and the phylogenetic analysis of voles of the generic group Microtus from the eastern part of the Greater Caucasus, including the Ismayilli, Khizi, and Balakan Districts of Azerbaijan, have been carried out. Three species, the Major's pine vole (M.majori), the social vole (M. socialis), and the common vole (M. arvalis form obscurus), have been identified, and five new haplotypes have been described for them. Genetic analysis with the inclusion of the new data showed that for each of the species, the physiographic conditions of the Greater Caucasus played a certain role (isolation, migration route or refugium) during the formation of the modern genetic structure. The obtained results indicate that any new data from the Caucasus could be of critical importance for the reconstruction of the evolutionary history of the modern biodiversity both within the region itself and in adjacent territories.

Здрібнення особин як стратегія популяцій в антропогенних умовах (досвід 50-річного вивчення популяцій гризунів)

Based on results of 50 years of continuous observations of populations of the pine vole (Microtus subterraneus de Selys-Longchamps, 1836) and yellow-necked wood mouse (Sylvaemus flavicollis Melchior, 1834), the phenomenon of reducing body size of individuals was revealed, particularly a significant reduction in body dimensions and body mass. The research was conducted at the Kaniv Nature Reserve covering various stages of the local ecosystem's existence under anthropogenic impact. Four cycles of density dynamics of two populations are chosen for comparison of their characteristics. The first three cycles correspond to qualitatively different periods in the existence of the protected ecosystem and populations of the studied species, whereas the last cycle reflects the current situation. It has been established that the tendency to decrease body dimensions is also characteristic for other rodent species, its manifestations are observed for 35 years, and the scale gradually increases. By fatness indexes, individuals of the pine vole on average lose 23.3% and yellow-necked wood mice lose 16.7% of the former values. It was shown that the level of reduce in exterior parameters is always greater in females than in males, and in the group of breeding adults it can reach 32%. It has been found that the phenomenon also applies to juveniles, whose fatness decreases by an average of 21%. The phenomenon occurs against the background of violations of various aspects of population dynamics, which allows it to be associated with anthropogenic changes in the environment. It is suggested that shrinking can be realized by various mechanisms. First, as a result of mortality, the largest individuals and reproductive females with their greatest energy needs fall out of the population, and, second, the growth and weight gain of young animals is slower. As a result, the decrease in external parameters of individuals reduces their specific energy needs and allows them to better survive under adverse conditions. From these points of view, reducing body dimensions can be considered as a specific population strategy to maintain ecological balance.

Diet of sympatric Barn Owls Tyto alba and Short-eared Owls Asio flammeus in an agricultural landscape in south-east Spain

The diets of the Barn Owl Tyto alba and the Short-eared Owl Asio flammeus have been extensively studied worldwide over the past few years, especially on the Iberian Peninsula. Nevertheless, very few studies have examined the diets and the trophic niche overlap in areas where these two raptor species occur in sympatry. As such, in this study we compared the diets of the Barn Owl and the Short-eared Owl inhabiting agricultural landscapes of the Vega de Granada, south-east Spain, based on pellet analysis. The diets were very similar, as both owls preyed mainly on small mammals, the Algerian Mouse Mus spretus being the prey most commonly found in pellets from both species. Although the diet of the Barn Owl was more diverse than that of the Short-eared Owl, the food niche overlap was very high, thus indicating a low interspecific trophic segregation. Despite the similarities between both diets, the frequency of the Mediterranean Pine Vole Microtus duodecimcostatus was much higher in pellets from the Barn Owl, thus suggesting that the Barn Owl may exert pest control in years when the Mediterranean Pine Vole occurs in high numbers.

Genetic variation at the p53 locus of two ecologically divergent Microtus pine voles: identification of molecular markers for species assignment.

The Lusitanian (Microtus lusitanicus) and the Mediterranean (Microtus duodecimcostatus) pine voles are recently diverged sister species endemic of the Iberian Peninsula that can be identified with ecological and morphological characters, but in areas where the 2 species co-occur, species designation may be difficult. Genetic discrimination between M. lusitanicus and M. duodecimcostatus has not been achieved yet possibly because of their estimated recent split and an evolutionary history that includes inter-species gene flow. Following our previous observations on exons 5-7 of the p53 gene, here we analyze the potential use of the p53 genomic region as a discrimination marker of these species by extending our analyses to several kb upstream and downstream of the p53 gene and characterizing the degree of genetic differentiation in 7 markers within this region. Additionally, we fully sequenced the P53 protein of both species. We observed: (i) generally high differentiation in this region; (ii) M. duodecimcostatus showed in general higher values of nucleotide and haplotype diversities; (iii) the concatenated phylogenetic tree separates the 2 species; (iv) the 2 P53 proteins only differ in 1 amino acid; (v) 4 of the markers, 2 in p53, one in Atp1b2, and another in Wrap53, contain species-specific genetic variation thus allowing a reliable discrimination between specimens from both species, irrespective of sampling location or introgression status. We provide additional data on the putative role of p53 in the evolution of these species and present researchers with a fast and cost-effective resource for M. lusitanicus and M. duodecimcostatus identification.

Diversity of small terrestrial mammals under different organic farming management in Mediterranean and Continental agriculture ecosystems

Diversity of small terrestrial mammals under different organic farming management in Mediterranean and Continental agriculture ecosystems

Ecological Analysis of the Helminth Community of Microtus lusitanicus (Gerbe, 1879) (Rodentia) in Asturias (NW Spain).

Simple SummaryThe Lusitanian pine vole is an endemic rodent of the Iberian Peninsula, which has a burrowing behaviour and prefers to live underground. It feeds on bark and roots causing severe damage to trees. In Asturias (NW Spain), this species is considered a pest causing economic losses in apple orchards, damaging the tree, and sometimes even causing its death. With the aim to shed light on the helminth community of this rodent pest species and to elucidate which intrinsic and extrinsic factors affect its helminth species, a faunistic-ecological study was carried out. For this purpose, our own collection of 710 voles from several orchards of various locations in Asturias was used. The results of the ecological study revealed the influence of climate variables, the year and season of capture, as well as the host age, on the diversity of the helminth community and the infection parameters of helminth species, underlining the importance of their life cycles. Our findings on the helminth community of the Lusitanian pine vole in Asturias could be used to improve the biological methods applied to control the population of this rodent pest.The Lusitanian pine vole, Microtus lusitanicus, an endemic fossorial rodent of the Iberian Peninsula, has a burrowing behaviour and prefers to live underground. It feeds on bark and roots causing severe damage to trees. In Asturias (NW Spain), where M. lusitanicus is considered a pest in several orchards, a faunistic-ecological study was carried out to describe the helminth community of this species and the main factors that could influence its helminth component species. For this purpose, our own collection of 710 voles from several orchards of various locations in Asturias was used. Eight helminth species, four cestodes and four nematodes, were found. Statistical non-parametric tests were used to analyse the effects of extrinsic and intrinsic factors on the diversity of the helminth community and species prevalence and abundance. The results show the influence of climate variables, the year and season of capture, as well as host age, on the diversity of the helminth community and the infection parameters of some helminth species, underlining the importance of their life cycles. In addition to shedding light on the helminth community of this rodent in Asturias, the results obtained could be used to improve the biological methods applied to fight the M. lusitanicus pest.